Skip to main content

Advertisement

SpringerLink
Log in

Identifying resilience mechanisms to recurrent ecosystem perturbations

  • Community ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The complex nature of ecological systems limits the unambiguous determination of mechanisms that drive resilience to natural disturbance or anthropogenic stress. Using eight-year time series data from boreal lakes with and without bloom formation of an invasive alga (Gonyostomum semen, Raphidophyceae), we studied resilience of phytoplankton communities in relation to recurring bloom impacts. We first characterized phytoplankton community dynamics in both lake types using univariate metrics of community structure (evenness, species richness, biovolume and Simpson diversity). All metrics, except species richness, were substantially altered and showed an inherent stronger variability in bloom lakes relative to reference lakes. We assessed resilience mechanisms using a multivariate time series modelling technique. The models captured clear successional dynamics of the phytoplankton communities in all lakes, whereby different groups of species were substituted sequentially over the ice-free period. The models also identified that G. semen impacts in bloom lakes were only manifested within a single species group, not across species groups, highlighting the rapid renewal of the phytoplankton communities upon bloom collapse. These results provide empirical support of the cross-scale resilience model. Cross-scale resilience could provide an explanation for the paradox that similar species richnesses are seen in bloom-forming lakes and reference lakes despite the clear difference between the community features of the two different sets of lakes investigated.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Allen CR, Gunderson L, Johnson AR (2005) The use of discontinuities and functional groups to assess relative resilience in complex systems. Ecosystems 8:958–966

    Article  Google Scholar 

  • Angeler DG, Moreno JM (2007) Zooplankton community resilience after press-type anthropogenic stress in temporary ponds. Ecol Appl 17:1105–1115

    Article  PubMed  Google Scholar 

  • Angeler DG, Viedma O, Moreno JM (2009) Statistical performance and information content of time lag analysis and redundancy analysis in time series modeling. Ecology 90:3245–3257

    Article  PubMed  Google Scholar 

  • Blomqvist P, Herlitz E (1998) Methods for quantitative assessment of phytoplankton in freshwaters, part 2 (Report 4861). Naturvårdsverket (Swedish Environmental Protection Agency), Stockholm

  • Brand FS, Jax K (2007) Focusing the meaning(s) of resilience: resilience as a descriptive concept and a boundary object. Ecol Soc 12(1):23. http://www.ecologyandsociety.org/vol12/is1/art23

    Google Scholar 

  • Carpenter SR, Brock WA (2006) Rising variance: a leading indicator of ecological transition. Ecol Lett 9:311–318

    Article  CAS  PubMed  Google Scholar 

  • Carpenter SR, Ludwig D, Brock WA (1999) Management of eutrophication for lakes subject to potentially irreversible change. Ecol Appl 9:751–771

    Article  Google Scholar 

  • Carpenter S, Walker B, Anderies JM, Abel N (2001) From metaphor to measurement: resilience of what to what? Ecosystems 4:765–781

    Article  Google Scholar 

  • Clegg MR, Maberly SC, Jones RJ (2007) Behavioural responses as a predictor of seasonal depth distribution and vertical niche separation in freshwater phytoplanktonic flagellates. Limnol Oceanogr 52:441–455

    Article  CAS  Google Scholar 

  • Cronberg G, Lindmark G, Björk S (1988) Mass development of the flagellate Gonyostomum semen (Raphidophyta) in Swedish forest lakes—an effect of acidification? Hydrobiologia 161:217–236

    Article  CAS  Google Scholar 

  • Cumming GS, Barnes G, Perz S, Schmink M, Sieving KE, Southworth J, Binford M, Holet DR, Stickler C, Van Holt T (2005) An exploratory framework for the empirical measurement of resilience. Ecosystems 8:975–987

    Article  Google Scholar 

  • Dray S (with contributions from P. Legendre and G. Blanchet) (2007) Packfor: forward selection with permutation (Canoco p. 46). R package version 0.0-8. http://vegan.r-forge.r-project.org/

  • Ellner S, Turchin P (1995) Chaos in a noisy world: new methods and evidence from time-series analysis. Am Nat 145:343–375

    Article  Google Scholar 

  • Eloranta P, Jarvinen M (1991) Growth of Gonyostomum semen (Ehr.) Diesing (Raphidophyceae): results from capture experiments. Verh Int Ver Theor Angew Limnol 24:2657–2659

    Google Scholar 

  • Eloranta P, Räike A (1988) Light as a factor affecting the vertical distribution of Gonyostomum semen (Ehr.) Diesing (Raphidophyceae) in lakes. Aqua Fenn 25:15–22

    Google Scholar 

  • Fath BD, Cabezas H, Pawlowski CW (2003) Regime changes in ecological systems: an information theory approach. J Theor Biol 222:517–530

    Article  PubMed  Google Scholar 

  • Figueroa R, Rengefors K (2006) Life cycle and sexuality of the freshwater raphidophyte Gonyostomum semen (Raphidophyceae). J Phycol 42:859–871

    Article  Google Scholar 

  • Findlay DL, Paterson MJ, Hendzel LL, Kling HJ (2005) Factors influencing Gonyostomum semen blooms in a small boreal reservoir lake. Hydrobiologia 533:243–252

    Article  CAS  Google Scholar 

  • Forys EA, Allen CR (2002) Functional group change within and across scales following invasions and extinctions in the Everglades ecosystem. Ecosystems 5:339–347

    Article  Google Scholar 

  • Garmestani AS, Allen CR, Mittelstaedt JD, Stow CA, Ward WA (2006) Firm size diversity, functional richness and resilience. Environ Dev Econ 11:533–551

    Article  Google Scholar 

  • Garmestani AS, Allen CR, Gallagher CM, Mittelstaedt JD (2007) Departures from Gibrat’s Law, discontinuities and city size distributions. Urban Stud 44:1997–2007

    Article  Google Scholar 

  • Garmestani AS, Allen CR, Gunderson L (2009) Panarchy: discontinuities reveal similarity in the dynamic system structure of ecological and social systems. Ecol Soc 14:15. http://www.ecologyandsociety.org/vol14/iss1/art15

    Google Scholar 

  • Gunderson LH (2008) Biophysical discontinuities in the Everglades ecosystem. In: Allen CR, Holling CS (eds) Discontinuities in ecosystems and other complex systems. Columbia University Press, New York, pp 83–100

  • Gunderson LH, Holling CS (2002) Panarchy: understanding transformations in human and natural systems. Island, Washington

  • Gunderson L, Allen CR, Wardwell D (2006) Temporal scaling in complex systems: resonant frequencies and biotic variability. In: Bissonette JA, Storch I (eds) Temporal dimensions of landscape ecology. Springer, Berlin, pp 78–89

    Google Scholar 

  • Hansson LA (2000) Synergistic effects of food chain dynamics and induced behavioral responses in aquatic ecosystems. Ecology 81:842–851

    Article  Google Scholar 

  • Hastings A (2001) Transient dynamics and persistence of ecological systems. Ecol Lett 4:215–220

    Article  Google Scholar 

  • Havlicek T, Carpenter SR (2001) Pelagic species size distributions in lakes: are they discontinuous? Limnol Oceanogr 46:1021–1033

    Article  Google Scholar 

  • Holling CS (2001) Understanding the complexity of economic, ecological and social systems. Ecosystems 4:390–405

    Article  Google Scholar 

  • Hongve D, Lovstad O, Bjorndalen K (1988) Gonyostomum semen—a new nuissance to bathers in Norwegian lakes. Verh Int Ver Theor Angew Limnol 23:430–434

    Google Scholar 

  • Janssen MA, Walker BH, Langridge J, Abel N (2000) An adaptive agent model for analysing co-evolution of management and policies in a complex rangeland system. Ecol Model 131:249–268

    Article  Google Scholar 

  • Kamykowski D, Yamazaki H (1997) A study of metabolism-influenced orientation in the diel vertical migration of marine dinoflagellates. Limnol Oceanogr 42:1189–1202

    Article  Google Scholar 

  • Le Cohu PR, Guitard J, Comoy N, Brabet J (1989) Gonyostomum semen a potential nuisance in large French reservoirs? The case of the Pareloup lake. Arch Hydrobiol 117:225–236

    Google Scholar 

  • Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280

    Article  Google Scholar 

  • Lepistö L, Antikainen S, Kivinen J (1994) The occurrence of Gonyostomum semen (Ehr.) Diesing in Finnish lakes. Hydrobiologia 273:1–8

    Article  Google Scholar 

  • May RM (1974) Biological populations with nonoverlapping generations: stable points, stable cycles, and chaos. Science 186:645–647

    Article  CAS  PubMed  Google Scholar 

  • Olrik KP, Blomqvist P, Brettum P, Cronberg G, Eloranta P (1989) Methods for quantitative assessment of phytoplankton in freshwaters, Part I. Swed Environmental Protection Agency, Stockholm

  • Peres-Neto PR, Legendre P, Dray S, Borcard D (2006) Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87:2614–2625

    Article  PubMed  Google Scholar 

  • Peterson GD (2002) Contagious disturbance, ecological memory, and the emergence of landscape patterns. Ecosystems 5:329–338

    Article  Google Scholar 

  • Peterson GD, Allen CR, Holling CS (1998) Ecological resilience, biodiversity, and scale. Ecosystems 1:6–18

    Article  Google Scholar 

  • Pickhardt C, Folt CL, Chen CY, Klaue B, Blum JD (2002) Algal blooms reduce the uptake of toxic methylmercury in freshwater food webs. Proc Natl Acad Sci USA 99:4419–4423

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Raffaelli D, Hall S, Emes C, Manly B (2000) Constraints on body size distributions: an experimental approach using a small-scale system. Oecologia 122:389–398

    Article  Google Scholar 

  • Rengefors K, Pålsson C, Hansson LA, Heiberg L (2008) Cell lysis of competitors and osmotrophy enhance growth of the bloom-forming alga Gonyostomum semen. Aquat Microb Ecol 51:87–96

    Article  Google Scholar 

  • Rondel C, Arfi R, Corbin D, Le Bihan F, Ndour EH, Lazzaro X (2008) A cyanobacterial bloom prevents fish trophic cascades. Freshw Biol 53:637–651

    Article  CAS  Google Scholar 

  • Rusak JA, Yan ND, Somers KM, McQueen DJ (1999) The temporal coherence of zooplankton population abundances in neighboring north-temperate lakes. Am Nat 153:46–58

    Article  Google Scholar 

  • Salonen K, Rosenberg M (2000) Advantages from diel vertical migration can explain the dominance of Gonyostomum semen (Raphidophyceae) in a small, steeply-stratified humic lake. J Plankton Res 22:1841–1853

    Article  Google Scholar 

  • Scheffer M, Brock W, Westley F (2000) Mechanisms preventing optimum use of ecosystem services: an interdisciplinary theoretical analysis. Ecosystems 3:451–471

    Article  CAS  Google Scholar 

  • Scheffer M, Rinaldi S, Huisman J, Weissing FJ (2003) Why plankton communities have no equilibrium: solutions to the paradox. Hydrobiologia 491:9–18

    Article  Google Scholar 

  • Smayda TJ (1997) Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol Oceanogr 42:1137–1153

    Article  Google Scholar 

  • Sommer U, Gliwicz ZM, Lampert W, Duncan A (1986) The PEG model of seasonal succession of planktonic events in fresh waters. Arch Hydrobiol 106:433–471

    Google Scholar 

  • Stow C, Allen CR, Garmestani AS (2007) Evaluating discontinuities in complex systems: toward quantitative measures of resilience. Ecol Soc 12:26. http://www.ecologyandsociety.org/vol12/iss1/art26/

    Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://cran.r-project.org

  • Wardwell DA, Allen CR, Peterson GD, Tyre AJ (2008) A test of the cross-scale resilience model: functional richness in Mediterranean-climate ecosystems. Ecol Complex 5:165–182

    Article  Google Scholar 

  • Wilander A, Johnson RK, Goedkoop W (2003) Riksinventering 2000. En synoptisk studie av vattenkemi och bottenfauna i svenska sjöar och vattendrag. Institutionen för Miljöanalys, SLU, Uppsala

Download references

Acknowledgments

The data used for this study form part of a long-term monitoring program financed by the Swedish Environmental Protection Agency. Additional support of DGA and SD by the Swedish EPA is acknowledged. CT acknowledges financial support from the Ramón Areces Foundation (Spain). Thanks to Jim Grover and the reviewers for helpful comments on the manuscript.

Author information

Authors and Affiliations

  1. Department of Aquatic Sciences and Assessment, Swedish University of Agricultural Sciences, PO Box 7050, 750 07, Uppsala, Sweden

    David G. Angeler, Cristina Trigal, Stina Drakare, Richard K. Johnson & Willem Goedkoop

Authors
  1. David G. Angeler
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cristina Trigal
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stina Drakare
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Richard K. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Willem Goedkoop
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David G. Angeler.

Additional information

Communicated by Ulrich Sommer.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 47 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Angeler, D.G., Trigal, C., Drakare, S. et al. Identifying resilience mechanisms to recurrent ecosystem perturbations. Oecologia 164, 231–241 (2010). https://doi.org/10.1007/s00442-010-1640-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-010-1640-2

Keywords

Search

Navigation